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Antibacterial Activity, Cytotoxicity and Chemical Constituents of Hydnora Johannis Roots

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Antibacterial Activity, Cytotoxicity and Chemical Constituents of Hydnora Johannis Roots Available online at www.sciencedirect.com South African Journal of Botany 78 (2012) 228–234 www.elsevier.com/locate/sajb Antibacterial activity, cytotoxicity and chemical constituents of Hydnora johannis roots S. Yagi a,b, F. Chrétien a, R.E. Duval c, S. Fontanay c, M. Maldini d, S. Piacente d, M. Henry a, ⁎ Y. Chapleur a, D. Laurain-Mattar a, a Groupe S.U.C.R.E.S., UMR 7565 CNRS-Nancy-Université, BP 239,54506 Nancy-Vandoeuvre, France b Botany Department, Faculty of Science, University of Khartoum, P.O. Box 321, Khartoum, Sudan c GEVSM, UMR 7565 CNRS, Nancy-Université, Nancy, France d Università degli Studi di Salerno, Dipartimento di Scienze Farmaceutiche, via Ponte don Melillo, 84084 Fisciano (Sa), Italy Received 17 March 2011; received in revised form 8 September 2011; accepted 14 September 2011 Abstract In Sudan, the roots of Hydnora johannis (Hydnoraceae) are traditionally used for the treatment of dysentery, diarrhea, cholera and swelling tonsillitis. The ethnomedicinal value of H. johannis was investigated through phytochemical study, in vitro antibacterial activity and preliminary cytotoxic tests. Determination of total phenols, flavonoids and proanthocyanidins was carried out using spectrometric methods. The antibacterial activity of the water and ethanolic extracts was determined using the microdilution method. Pure compounds were isolated from the ethyl acetate extract by chromatographic methods and their structures were established by spectroscopic methods. Cytotoxicity assay was performed against selected human mouth epidermoid carcinoma cell line (KB), and non-cancer human fetal lung cell line (MRC-5). Both water and ethanol (70%) extracts were found to contain the same amount of total phenols and proanthocyanidins, whereas the level of flavonoids was higher in the ethanol extract. The water extract was found to possess antibacterial activity against Enterococcus faecalis (MIC value of 16 μg/mL), Bacillus subtilis, B. cereus and Staphylococcus aureus (MIC values of 64 μg/mL) but not against bacteria mainly responsible for diarrhea. This leads to the suggestion that, the mode of action of water extract which is rich in tannins was not connected to their inhibition to the diarrhea bacteria but to their action on the digestive tract. Reduction in potency of the water and ethanol (70%) extracts when fractionated was observed. The ethyl acetate frac- tion obtained from fractionation of ethanol extract possessed only activity against the two strains of S. aureus with MIC values of 128 μg/mL. In addition, six compounds were isolated from the ethyl acetate extract as cirsiliol (3′,4′,5-trihydroxy-6-7-dimethoxy flavone) (1), trans 3′5-dihy- droxy-4′7-dimethoxydihydroflavonol (2), oleic acid (3), vanillin (4-hydroxy-3-methoxybenzaldehyde) (4), protocatechuic acid (3,4 dihydroxy benzoic acid) (5) and dl catechin (trans (+) 2-(3,4-dihydroxyphenyl-3,4-dihydro-2H-1-benzopyran-3,5,7-triol)) (6). Four compounds from the ethyl acetate extract were also identified by GCMS as stigmasterol (7), oleic acid (3), myristic acid (8), and palmitic acid (9). Little cytotoxicity is reported against the cell lines used. Thus, the safety of this plant in the traditional medicine should be verified by much further testing, including in vivo experiments and clinical studies. © 2011 SAAB. Published by Elsevier B.V. All rights reserved. Keywords: Antibacterial activity; Chemical constituents; Cytotoxicity; Hydnora johannis 1. Introduction reported that diarrhea is the highest course of infant mortal- ity disease in the world, occurring mostly in developing Diarrhea has long been recognized as one of the most im- countries (Murray et al., 2001). It is a major health concern portant health problems in developing countries. It has been in developing countries and remains an important clinical problem even in developed countries despite improvements ⁎ in public health and economic wealth (Casburn-Jones and Corresponding author. – E-mail address: [email protected] Farthing, 2004). It is estimated that during the next 20 (D. Laurain-Mattar). 30 years, diarrhea along with other infectious diseases will 0254-6299/$ - see front matter © 2011 SAAB. Published by Elsevier B.V. All rights reserved. doi:10.1016/j.sajb.2011.09.010 S. Yagi et al. / South African Journal of Botany 78 (2012) 228–234 229 remain a cause of global health concern (Meyrowitsch and 2. Material and methods Bygbjerg, 2007). Treatment of diarrhea is generally non- specific and is usually aimed at reducing the discomfort and 2.1. Plant material inconvenience of frequent bowel movements (Brunton, 1996). To overcome the menace of diarrheal diseases in devel- Roots of H. johannis were collected from Aldamasin district of opingcountries,theWorldHealthOrganization(WHO)has The Blue Nile Region, Sudan in January 2006. The plant was iden- included a program for the control of diarrhea, which involves tified and a voucher specimen no 41936HBD was deposited in the the use of traditional herbal medicine (Atta and Mouneir, Herbarium of Botany Department, Faculty of Science, University 2004; Snyder and Merson, 1982). Therefore, it is necessary of Khartoum for future reference. to establish the scientific basis for the therapeutic actions of traditional plant medicines. Several plants have been reported 2.2. Preparation of extracts to be used in treating and managing diarrheal diseases (Agunu et al., 2005). Traditional medical practitioners play important Two main types of extracts (water and ethanol) were prepared roles in health care delivery in Sudan. With recent increasing and then were further subjected to different fractionations. Water interest in alternative/herbal medicine for the prevention and extract (WE) was prepared by simple maceration of 500 g of treatment of various illnesses, there is an increasing concern powdered roots in 1500 mL of distilled water maintained at am- about the safety of medicinal plants. In Sudan, toxicoses bient temperature for 4 h. Extract was first filtered on filter with medicinal plants are encountered among the village paper, then centrifuged for 15 min at 0.704×g and finally populations who are dependent mainly on traditional medi- freeze-dried to yield 13.56 g of WE. In order to get water fraction cine. Most cases of poisoning result from over dosages be- not containing tannins, the method of tannin separation using rab- cause, in general, there is no standardized dosage system in bit leather described in the European Pharmacopeia (edition traditional medical practice (Saad et al., 2006). To ensure re- 2005) was adopted. Two grams of WE was dissolved in producible quality of herbal products, preliminary validation 200 mL distilled water. Two grams of rabbit leather powder (pur- in laboratory and an optimization of their formulation are ut- chased as substance R according to the purity criteria mentioned most essential. in the European Pharmacopeia) was added and the mixture was The Hydnoraceae with only two genera Hydnora and put under agitation for 1 h at room temperature, and then filtered. Prosopanche include some of the strangest plants in the To insure the absence of tannins from the filtrate, 200 μLof world. The vegetative plant body is highly reduced consist- FeCl3 (10%) were added to 1 mL of filtrate. A dark violet color ing of only roots, flowers and fruits. In fact, the Hydnora- is developing in the presence of tannins. The filtrate was repeat- ceae are the only known angiosperm with no leaves or edly extracted by rabbit leather powder until tannins were absent. scales of any sort (Musselman, 1991). There are currently Filtrate free of tannins was freeze dried to yield 0.24 g of non- five species recognized; H. johannis Becc. (=H. abyssinica tannins water extract (NTWE). Tannins fraction (TF) was sepa- A. Br. =H. solmsiana Dinter), H. africana Thunb., H. escu- rated from rabbit leather powder by adding 5 g of trypsin to the lenta Jum. and H. Perrier, H. triceps Drège and E. Mey. and complex (tannins+rabbit leather) under light agitation at 37 °C H. sinandevu Beentje and Q. Luke (Tennakoon et al., 2007). for 36 h. The supernatant was extracted with phenol:chloro- H. byssinica occurs from northern Namibia, across most of form:ethanol (25:24:1 (v/v/v)) to get rid of the protein and then Angola and the DRC, to Ethiopia, Sudan and the Arabian freeze dried to yield 9.94 g of TF. The ethanolic extract was pre- peninsula (Bolin et al., 2005; Musselman and Visser, pared by soaking 2 kg of roots powder in 70% ethanol at ambient 1989). Moreover, recent studies demonstrated its occurrence temperature for 5 days. The extract was decanted, filtered under in South Africa (Williams et al., 2011a), as well as Mozam- vacuum, concentrated in a rotary evaporator, then extracted suc- bique and Malawi (Williams et al., 2011a, 2011b). H. johan- cessively with n-hexane (250 mL×3), CHCl3 (300 mL×3), and nis is found parasitizing the roots of Acacia nilotica EtOAc (300 mL×3) and were evaporated under reduced pressure (Musselman and Visser, 1987). The plants are reportedly to yield 1.16 g, 3.50 g and 5.60 g residues respectively. The water used to treat diarrhea, piles, acne, menstrual problems, stom- extract (70.6 g) left was lyophilized. ach cramps and to stop bleeding (Dold and Cocks, 2003; Hutchings et al., 1996; Musselman and Visser, 1989). In 2.3. Determination of total phenolics Sudan, decoction of the roots of H. johannis is traditionally used for the treatment of dysentery, diarrhea, cholera and Water and ethanol extracts were resuspended separately in swelling tonsillitis (El Ghazali, 1997). Phytochemical stud- ethanol to make 50 mg/mL stock solutions. Total phenol contents ies and biological evaluation of this plant are scanty. Con- in the extracts were determined using modified Folin–Ciocalteu sidering the widespread use of H. johannis in some parts method (Wolfe et al., 2003). An aliquot of the extract was of Sudan, the present study was conducted to assess the pos- mixed with 5 mL Folin–Ciocalteu reagent (previously diluted sible antibacterial activity and toxic effect of the roots of with water at 1:10 v/v) and 4 mL (75 g/L) of sodium carbonate.
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